Viruses of Shade Trees

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22 5

JOURNAL OF

ARBORICULTURE

September 1980

Vol .

6, No. 9

V IRUS AND V IRUS-LIKE DISE ASE S OF SHADE TRE E S

1

by D.F. Millikan

The number of known virus diseases affecting

shade trees is limited. This may reflect limited

observations rather than limited disease occur-

rence. The pressure for research on the more

economically important food and fiber crops has

stifled needed research on plants grown for

esthetic purposes. Trees are continuously ex-

posed to possible infection by viruses; therefore,

it is surprising that so few have been found. Trees

may be infected but the expression of the symp-

oms is so mild that they are not readily recog-

nized. However, the presence of viruses in

ature trees showing no obvious symptoms has

een demonstrated in Australia. An entomologist

ucalyptus trees and caged these on young

wide range of symptom s

When a shade tree is infected with a virus the

virus.

The leaves of birch trees

sion and these symptoms disappear with applica-

tions of boron sprays. Pin oaks often have

dwarfed, distorted leaves in mid-spring. Such

foliar malformations are characteristically those

associated with virus infection but may be due to

2,4-D injury. Leaves of pin oaks growing on

shallow soils, generally with a high calcium con-

tent and an alkaline pH, frequently become

chlorotic to completely yellow with necrotic

margins. Since the agent causing this disorder can

not be transmitted and the affected trees respond

to applications of iron chelate, pin oak chlorosis

has been show n to be due to lack of availableiron.

Witches' broom is so prevalent and species-

specific that it is often used to identify hackberry.

These symptoms are typical for virus-like

disorders, but this disease is caused by a mite-

mildew complex. Bunch on walnut is another

witches' broom type of disease. This disorder af-

fects black walnut

{Juglans

nigra),English or Per-

sian walnut (J. regia), butternut (J. clnerea),and

heartnut (J. sieboldiana var. cordiformis)with the

severity of the disease increasing in an ascending

order from symptomless to mild on black or Per-

sian walnut to death of heartnut. Although the in-

criminating agent has not been isolated in pure

culture, electron micrographs and remission

studies with tetracycline place it in the diseases

incited by the mycoplasma-like organisms (MLO).

Diseases Caused by Mycoplasma-Like

Organisms MLO)

Few transmissible diseases possess symptoms

as spectacular as witches' broom or yellows.

Previous to 1967, such diseases were con-

sidered to be of a virus etiology, since these could

Journal Paper 8 28 5, Approved by the Director.


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22 6

Millikarv. Virus

MLO D iseases

be transmitted by grafting, dodder, and/or leaf

hoppers. None of these disorders could be

transmitted mechanically nor were there virus par-

ticles detected by electron microscopy. In 1967,

however, Doiet al.(5) found ploeomorphic bodies

in the phloem elements of several of these wit-

c h e s ' b r o o m an d y e l l o w s d i s o r d e r s .

Simultaneously, Ishiie et al. (13) found that ap-

plications of tetracycline would suppress symp-

toms of these disorders. The morphological

similarity of these ploeomorphic bodies to the

mycoplasma-inciting animal diseases was striking.

Further evidence of similarity w as the suppression

of symptoms by tetracycline. MLO's have been

isolated in pure culture only in two cases;

therefore , until the incriminating organisms can be

cultured,

those diseases with a mycoplasma-like

etiology based on electron microscopy and remis-

sion by tetracyclines are considered as MLO-

induced diseases.

Ash witches' broom was first reported in New

York (1 1) where an occasional tree in a population

of declining white ash showed symptoms of a

yellows-type disease. These symptoms included

small and chlorotic leaves, shortened internodes,

and shoot growth from axillary and terminal buds

which normally remain dormant until the following

growing season. The transmissibility of this

disorder (14) was demonstrated by attaching

apical cuttings (5-10 cm) of dodder, Cuscuta

subinclusa, grown from seed and maintained on

tobacco, on witches' broom shoots. The shoots

with attached dodder were enclosed within a

plastic bag con taining a screened ventilation to ex-

clude insects. Eight weeks after establishment,

apical cuttings of this dodder were removed and

attached to healthy Vinca rosea. Symptoms of a

yellows-type appeared on these Vinca four to five

months later. Transmission to other healthy Vinca

by cleft grafting resulted in a reproduction of

symptoms while dodder attached to carrots

resulted in the appearance of symptoms typical of

those described for yellows diseases by Kunkel

(15).

Electron micrographs confirmed the

presence of MLO in the mature sieve tubes of

midveins and pe tioles of diseased ash, carrot, and

Vinca.

Witches' broom of black locust was found in

1898 (24) when the typical brooming symptoms

appeared on locust stump sprouts in Maryland.

This was later transmitted by grafting. Symptoms

included the proliferation of shoots and a reduced

size of leaves with the broom always being erect

or ascending. Occasionally a cushion 4-5 cm in

diameter and about 1 cm thick formed on the

trunk. This cushion bore groups of buds and tiny

leaves on its surface and represented an extreme

form of bunch. Brooming is frequently found on

sprouts a rising from the roots and stumps of trees

which were symptomless prior to cutting. These

generally show little resemblance to comparable

healthy locust growth. Frequently, the broom

develops terminally or in the axils of normal leaves

near the top of the sprout. The presence of MLO

in the sieve elements and companion cells of the

phloem of stems, roots, and petioles of black

locust with witches' broom symptoms places this

disease in the MLO type of disorder. This disease

is rather widespread in eastern USA and has been

reported in Europe.

Bunch on walnut (Fig. 1) was reported by Waite

in 19 32 (23) and described in detail by Berry (3).

Symptoms include a curling, cupping, chlorosis,

and narrowing of the leaflets on small, wiry

shoots. The bunch symptoms result from the

development of shoots from buds on the primary

stems in mid to late summer. Ordinarily these buds

remain dormant until the following spring. These

shoots are juvenile and succulent and do not

become dormant in the late

fall,

thus, generally

winter-kill. This annual late summer growth and

subsequent dieback is so severe on some heart-

nut cultivars that they are killed within two years.

Circumstantial evidence suggests that different

strains of the bunch MLO exist. A single tree of

the heartnut cultivar, Stranger, showed marked

brooming but later completely recovered (R.

Oaks, unpublished data). Bunch was considered

to have a virus etiology until MLO's were found

(16,20) in the sieve tubes of leaf, stem of root

phloem cells.

Lethal yellows of palm is a destructive disease in

Florida and the Caribbean region. It was describe d

by Carter et al. (4) who indicated that yellowing

was a general symptom which covered other

disorders as well. Mechanical damange or a


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Journal of Arboriculture 6(9 ): September 19 8 0

2 27

localized conce ntration of scale insects can cause

tip yellow ing, which is a specific symptom that can

cause temporary confusion. Leaflets near the tips

of fronds in the middle of the crown become b right

yellow at, or just after, nutfall. The number of

yellowed tips per frond varies from 1-11 and may

involve a few leaflets or as much as half the length

of the frond. In about four weeks these symptoms

progress to complete death of the frond. Infre-

quently, patch yellows occurs, first appearing in

3-7 leaflets in the middle of the frond. On a ffected

fronds the color spreads both ways and the

leaflets dry up in about four weeks. A general

yellowing is another symptom. This starts in one

or more of the oldest fronds and progresses

towards the center of the frond. These yellowed

fronts (approximately % of the crown) will fall off in

about two weeks. The remaining fronds of the

crown may remain intact for about four, months,

then turn yellow changing to brown when the en-

tire crown breaks off. Final diagnosis of lethal

yellows is based on the appearance of a blacken-

ed inflorescence. The spathe may open normally

with a fully developed inflorescence, then the tips

of the male spikelets turn brown or black. The

number of spikelets showing this dark color vary

from one to all within the inflorescence and this

discoloration continues downward. The necrosis

progresses to include the female flowers and

within four weeks the entire inflorescence

blackens. This process accelerates and involves

all of the emerging spathes. The basal portions

rot, leading to death of the tree.

Fig.1 . Typical bunch symptoms on w alnut caused by MLO

courtesy, C .E. Seliskar).

Cole (4) considers the brooming of branches

and shoo ts as the most distinguishing symptom of

pecan bunch. Bunch may appear on small and/or

large branches and on sucker growth. Axillary

buds of the current year's growth develop laterals

which often equal the length of the primary shoot.

Lateral buds on the lateral shoots also may be

forced into gro wth. In advanced stages of bunch,

the new sho ots are short and slender but the buds

are weak and may fail to deve lop. The color of the

leaves on these witches' brooms varies from dark

green to chlorotic. The width of the terminal

leaflets are narrower. The leaflets usually arethin-

ner and wider but abscise in late summer or early

fall,starting w ith the lower leaves and progressing

upwards. Leaflets on the broom appear earlier

than those on the healthy trees. Production of

nuts is reduced on the severely affected trees and

the nuts may be small and poorly

filled.

The

presence of MLO's in the phloem elements of the

twigs and petioles adds pecan bunch to our grow-

ing list of diseases caused by MLO's.

Swingle (21) described phloem necrosis of elm

in 1938 after

an

extensive dying of American elms

in the central and lower Ohio rivershed. Symp-

toms of phloem necrosis first appear in the ex-

treme tips of branches. Foliage becomes thin and

the leaves droop due to the downward curvature

of the petioles. The leaf blades curl upwards at the

margin,producing a trough-like effect that makes

the leaves appear narrow and greyish-green.

Such leaves are often stiff and brittle. Later, the

foliage becomes yellowish-green and finally

yellow, followed by dropping. These symptoms

occur throughout the entire crown. In advanced

stages the roots die with the small, fibrous ones

succumbing first. Typical discoloration, confined

to the phloem and cambium, precedes death of

the larger roots and frequently may be found ex-

tending into the trunk and branches. In large

trees,

this discoloration usually occurs in large

roots at the base of the trunk , just before death of

the tree. The cambium first becomes light yellow

or golden followed by a yellowing of the phloem

which turns butter-scotch brown with small, scat-

tered black flecks. Soon thereafter the phloem

becomes dark brown and necrotic and produces

an odor resembling wintergreen.


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Millikan:

Virus

MLO Diseases

Table 1. Transmissible diseases of trees with a MLO etiology

Common name

Ash witches broom

Brooming of black locust

Bunch of walnut

Lethal yellows of palm

Pecan bunch

Phloem necrosis of elm

Type

yellows

yellows

yellows

yellows

yellows

Host

Fraxinus amerlcana

Robinia pseudoacacia

Juglansspp.

Cocosnucifera

Carya illinoensis

Ulmus americana

Reference

Hibben & Wolanski, 1 97 0. Phytopathology

60:1295 (Abstr.)

Seliskar et

al.

1973. Phytopathology 63:30

Hutchins & Wester. 19 47 . P hytopathology

37:11 (Abstr.)

Plavsic-Banja et a/. 1972. Phytopathology

62 :298 .

Seliskar et al. 1974. Phytopathology

64 :1269 .

Wilson et al. 1972. Phytopathology

62 :140 .

Economical implications. Lethal yellows of

palm is rapidly killing the coconut palms in south

Florida and the Caribbean. This disease responds

to tetracycline therapy but this is practical only for

lawn and avenue trees and then only to provide

time for the planting and growth of resistant

clones. Brooming of black locust appears to be

widespread east of the Mississippi River, thus, the

wisdom of planting this species in those areas

where the disease is endemic seems ques-

tionable. The similarity of bunch symptoms on

pecan and walnut suggest that the same, or

strains of the same, MLO may be responsible.

Both the heartnut and butternut are so susceptible

to bunch that they should not be planted in areas

where bunch is present. There is circumstantial

evidence that bunch is responsible for a heavy

mortality of butternuts in southern Minnesota,

thus,

m ore information on the spread and the vec-

tor responsible is critically needed. Neither ash

witches' broom nor phloem necrosis of elm ap-

pear to be serious diseases at this time. The

former has a rather restricted range but could

become a real threat should environmental

changes occur which would result in a rapid

spread.W ith the devastating spread of Dutch elm

disease (DED), phloem necrosis seems unimpor-

tant. The disease, however, is spreading in those

areas which are still free from DED. This disease

should be taken into consideration in current

breeding programs for resistance to DED.

Diseases C aused by V iruses

The list of viral infections on shade trees is less

imposing than that of the M LO's but this may be a

function of visibility and persistence. Unlike the

diseases caused by MLO's where brooming and

yellowing are obvious and persist, the symptoms

of virus infections often are mild and, in many

cases, become latent after passing through the

shock phase. Only when these diseases con-

tribute to unmistakable loss of vigor or death and

the symptoms are recurrent and clearly visible, do

we recognize these disorders. Nonetheless, as

our interests in landscape and environmental con-

cerns increase, this list will grow.

Amelanchier mottle was reported in 1956 (18)

when a bud from an apple tree showing symptoms

of severe stem pitting (9) was placed into a shad

bush,

Amelanchier spp. Thirteen months later

when the shoots of the shad bush were 10 cm

long,

a striking mottle (Fig. 2) appeared on the

leaves of the shoot above the inserted apple bud.

These leaves were dwarfed and rugose, in sharp

contrast to the smooth leaves on the adjoining

healthy clone. The identity of the virus causing

this mottle was not established but the presence

of ch lorotic leaf spot (CLSV) in the inocula and the

similarity of symptoms on other indicators (19)

suggest that CLSV was responsible.

Ash dieback featuring a progressive dying back

of the branches and ultimate death of the ash tree

has been a serious problem in the northeast for

several decades. Dieback is particularly serious

on white ash, raxinus americana,but occasional-

ly is found on green ash, F. pennsylvanica var.

lanceolata.In 19 63 and 19 64 , Hibben (11) found

virus-like symptoms on the leaves of white ash in

all stages of branch dieback. These sym ptoms in-

clude faint chlorotic spots and rings, irregular


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229

2. Mo ttle on melanchierspp. thirteen m onths after in-

om inoculated tree. Right, leaves of healthy

eaves showing chlorotic or reddish spots and

Additional transmission from bean to bean

Elm mosaic was first described by Swingle e t

al.

the vicinity of Cleve land, Ohio. Prior to the rapid

n size and texture . O thers are abnormally

stiff, and frequently dwarfed with a yellow

may account for its widespread o ccurrence

prior to the onset of DED.

Epinasty of flowering cherry is not a serious

disease due to its tendency for latency and the

lack on a known vector. Initially, this epinasty was

thought to be due to the ringspot virus (17). After

it was shown to be caused by the green ring mot-

tle virus, the cultivar, Kw anzan, has been used as

a virus indicator in state certification programs.

This epinasty ranges from mild to severe, depend-

ing upon the virus strain. Portions of the midvein

or lateral veins become necrotic, resulting in a

twisting and curling of the leaves, similar to that in-

duced by aphid feeding. Internodes of the

elongating terminals are shortened and as the

bark matures, it may be roughened by the

development of fissures. Terminal growth

becomes symptomless in early summer as the

temperatures become elevated.

Birch decline is a serious disease in north-

eastern USA and eastern Canada, affecting both

white and yellow birch (Betula papyrifera andB.

alleghaniensis). Most of the merchandable trees in

the severely affected areas were killed in the

1935-55 period. Hansbrough (10) in 1953

transmitted a gold ringspot of white birch to seed-

lings but did not associate this virus with the

decline. Later Berbee (2) transmitted the line pat-

tern of yellow birch to seedlings. The line pattern

symptoms on both species consist of chlorotic

lines forming oak-leaf designs, irregular rings or

linear flecks, sometimes accompanied by a mild

mosaic. Until fully expanded, emerging leaves on

infected trees generally are symptomless and

some infected trees have a few, or no, foliar

symptoms. These symptoms may be restricted to

a few leaves on a few branches. The leaves re-

main on the trees until the end of the growing

season.

Chlorotic tissue turns nearly white during

midsummer. The virus has been mechanically

transmitted to Chenopodium, co wpea , cucumber,

squash,

and bean. Serological and host range

studies demonstrate that this virus-causing line

pattern of birch is a strain of apple mosaic.

Palm mosaic, affecting Mexican fan palm,

Washingtonia robusta, is a recently described

disease of probable virus etiology. This palm is a

hardy, relatively disease-resistant species used

extensively in the warmer parts of California as an


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Millikan:

Virus MLO Diseases

ornamental. This disease became a problem when

a mosaic pattern was found on several small fan

palms in a retail nursery. Symptoms cons isted of a

bright mosaic on leaves (Fig. 3A) that were re-

duced in size. On the older leaves, the obvious

mosaic symptoms disappearandbright yellow and

ring patterns develop. Limited observations in-

dicate that infected trees have reduced growth

rates.

While mechanical transmission has not

been succes sful and no insect vectors have been

identified, electron micrographs revealed the

presence (Fig. 3B) of long, flexuous rods (686 X

13 nm) in the diseased material. No rods were

found in the healthy preparations. An examination

of thin-sectioned leaf material confirmed the

presence of p inwheel inclusion bodies,

characteristic of viruses belonging to the potato Y

group.

Zonate canker of elm is a virus disease of shade

trees that should be relegated to history. This

disease has been found in New J ersey, Ohio, and

Missouri either alone, or in combination with elm

mosaic. Although the foliar symptoms are similar

to those of elm mosaic, the symptom s differ in that

on inoculated trees leaves develop necrotic

spots in the first flush of growth. These are later

shed. Zonate canker also causes small, necrotic

cankers to deve lop on the bark of the upper stems

and branches of the inoculated trees. In old,

established trees it may appear as a latent infec-

tion with little or no obvious symptoms.

Economic importance.

Two of the viruses,

epinasty of flowering cherry and mottle on

Amelanchier, have little, if any, economic impor-

tance. Flowering cherry infected with the epinasty

virus can serve as a reservoir for infection of

peach or cherry but the lack of a known vector

minimizes this danger. Mottle on Am elanchierhas

been found only on experimentally inoculated

plants. Zonate canker of elm also is unimportant,

since most of the susceptible elms have been

replaced w ith other species . Elm mosaic also is no

longer a serious disorder but its causitive entity,

TomRSV, is a soil-borne virus with a wide host

range. Certainly any replacement species should

not be susceptible to TomRSV. The limited

distribution of ash ringspot indicates that this

disease presently is not serious. Ash ringspot,

Fig.

3. Palm mo saic courtesy, D.E. Mayhew). upper)

Mosaic patterns on leaves of infected Mexican palm,

Washingtonia robusta

W endl . midd le ) E l ec t ron

micrograph showing lo ng, flexuous rods 686 x 13 nm).

lower) E lectron micrographs showing pinwheel inclusio n

bodies.


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al of Arboriculture 6(9 ): September 19 80

2 31

Disease

ttle

m mosaic

diseases of trees with

Amelanchierspp.

Fraxinus americana

Ulmus americana

Prunus serulata

Betula papyrifera;

B. alleghaniensis

Washingtonia robusta

Ulmus americana

a virus etiology

1

Identity

CLSV

TRSV

TomRSV

QRMV

ApMV

PVY

Reference

Millikan & Guengerich. 1956.

Phytopathology 46:130

Hibben.

1966. Phytopathology 56:323

Swingle efal. 1943. Phytopathology

33 :1196

Fridlund & Deiner. 1 958. Plant Dis. Rptr.

4 2 : 8 3 0

Gotlieb & Berbee. 1973. Phytopathology

6 3 : 1 4 7 0

Mayhew & Tidwell. 1 97 8. Plant Dis. Rptr.

6 2 : 8 0 3 .

Swingle & Bretz. 1950. Phytopathology

4 0 : 1 0 1 8 .

Abbreviations used in this table are as follows: ApMV = apple mosaic virus; CLSV

=

tomato ringspot virus; TRSV = tobacco ringspot virus.

soil-

As indicated in Table 3, there are several

symptoms strongly indicate their

The economic importance of sugar maple in the

s disorder. Although sassafras is not one of our

and unattractive m ottling of the foliage ac-

chlorotic leafspot virus; GRMV = green ring mottie virus; PVY = potato virus Y; TomRSV

evidence of the potential seriousness of this

disease.

Fig.4. Mosaic on persimmon.

Table 3. Tree diseases of unknown etiology

under current investigation.

Disease

Host Reference

Maple variagation Acer saccharum Gotlieb, unpublish-

ed data

Persimmon mosaic DiospyrusvirginianaMillikan ef al . , un-

published data

Sassafras bunch

Sassafras

albidum Millikan ef al.,u n-

published data

Summary

The number of known transmissible virus and

virus-like disorders on shade trees is limited at the

present time. Since three of the disorders were


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232

Millikan:

Virus

MLO Diseases

described on American elm, the list is even less

impressive. Those with a MLO etiology outnumber

those with a viral nature and one of these, lethal

yellows of palm, is eliminating one species of

coconut in South Florida and the Caribbean

region. Bunch of walnut and pecan along with

brooming of locust also appear to be widespread

but their effects on the host vary from none, or lit-

tle, to death, depending upon the clone. Among

the diseases of a virus etiology, two occur on

hosts inoculated with known fruit tree viruses.

Line pattern of birch affects two species ofBetula

and is associated with a decline which is

eliminating these species in their natural habitat of

northeastern USA. Neither ash ringspot nor elm

mosaic are considered as serious diseases at the

present time. Since these diseases are caused by

strains of TRSV and TomRSV, are nematode-

transmitted and have a wide host range, they may

cause disease to other hosts.

Literature Cited

1.

Agrios, G.N. 1975. Virus and mycoplasma diseases of

shade and ornamen tal trees.J. Arboric. 1:41 -47.

2. Berbee, J.G. 1959. Birch dieback: Present status and

future needs, pp. 1555-1559. IN Recent advances in

botany II. Univ. of Toronto Press.

3. Berry, F.J. 1955. Walnut bunch disease. State of Calif.:

Dept. of Agriculture Bull. 44(2):63-67.

4. Bretz, T.W. 1944. Phloem necrosis of elms in Missouri.

Plant Dis. Reptr.

28 :929 -931 .

5. Carter, W., R.W. Latta, and J.R.R. Suah. 1965.Thesymp-

toms of lethal yellowing d isease of coconut palms.Food

Agr. Organ. UN Plant Protect. Bull. 13:49-55 .

6. Cole, J.R. 1937. Bunch disease of Pecan.Phytopathology

27:604 612

7. Doi, Y., M. Teranaka, K. Yora, and H. Asuyana. 1967.

Mycopiasma of PLT group-like microorganism s found jn

the phloem elemen ts of plants infected with mulberry

dwarf

potato witches broom, aster yellows, or

paulowinia witches broom. Ann. Phytopath. Soc. Japan

33 :259 -266 .

8. Fulton, J.P. and R.W. Fulton. 19 70. A com parison ofsome

properties of elm mosaic and tomato ringspot viruses.

Phytopathology 60:114-11 5.

9. Guengerich, H.W. and D.F. Millikan. 1956.Transmissionof

the stem pitting factor in apple. Plant Dis. Rptr.

40 :934 -938 .

10.Hansbrough, J.R. 1953. The significance of the fungi and

viruses associated with the birch decline. Report of the

Symposium on Birch Decline. Can. Dept. of Agr. Forest

Div. Ottawa.

11. Hibben, C.R. 1966.Transmissiono fthe ringspot-like virus

from leaves of w hite ash. Phytopathology 56:323-325.

12. Hibben, D.R. and B. Wolanski. 1971. Dodder transmis-

sion of a mycoplasma from ash witches broom.

Phytopathology 61: 151 -156 .

13.

Ishiie, T., Y. Doi, K. Yora, and H. Asuyama. 1967.Sup-

pressive effect ofantibioticson symptom development of

mulberry dwarf disease. Ann. Phytopath. Soc. Japan

33 :267 -275 .

14.Jackson,

L W R

and C. Hartley. 1933.Transmissibilityo f

the brooming disease of black locust. Phytopathology

23:83-90 .

15. MacDaniels, L.H., W.T. Johnson, and E.J. Braun. 1975.

The black walnut bunch syndrome. Northern Nut

Growers Assoc. Ann. Rept. 66:71-85.

17.

Milbrath, J.A. and S.M. Zeller, 1945. Latent viruses in

stonefruit. Science 101:114-115.

18. Millikan, D.F. and H.W. Guengerich. 1956. Transmission

to Amelanchier of

an

agent causing a disorder on apple.

Phytopathology 46:130.

19.Mink, G.I. and J.R. Shay. 1959. Preliminary

evaluation

of

some Russian apple varieties as indicators for apple

viruses. Suppl. Plant Dis. Rptr. 254:13-17.

20. Seliskar, C.E. 1973. Association of a mycoplasma-like

organism with walnut bunch disease. IN Abstracts of

papers, 2nd Int. Congr. Plant Pathology, paper 0933.

2 1 . Swingle, R.U. 1938. A phloem necrosis of elm.

Phytopathology 28:757-759.

22. Swingle, R.U., P.E. Tilford, and D.F.

Irish.

1 9 4 1 . A

transmissible mosaic of elm. Phytopathology 13:22.

(Abstr.)

23.

Waite, M.B. 1932. Notes on some nut disease with

special reference to the black walnut. Northern Nut

Growers Assn. Ann. Rept. 23:60-67.

2 4. Waters, C.E. 1898. Witches broom on locust. Plant

World 1:83-84.

25.

Wilkinson, R.E. 1952.Woody plant hosts of the tobacco

ringspot virus. Phytopathology 42:478. (Abstr.)

Department of Plant Pathology

University of Missouri

Columbia, Missouri

Viruses of Shade Trees

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